2.2 Study 2: Plant investment in arbuscular mycorrhizal fungi for N and P acquisition
2.2.6 Acknowledgments
We thank the Chilean National Park Service Corporación Nacional Forestal (CONAF) for the permission to work in the National Park La Campana and the National Park Nahuelbuta as well as the Comunidad Agrícola Quebrada de Talca for the possibility to work in the local ‘exclusion area for studying biodiversity and conservation’. We also thank Karin Schmidt for her support with lab analyses as well as the whole team of the Centre for Stable Isotope Research and Analysis (KOSI).
This study was funded by the German Research Foundation (DFG) [project number KU 1184/36-1, GO 896/13-1184/36-1, and DI 2136-11] within the Priority Program 1803 ‘EarthShape – Earth Surface Shaping by Biota’. We thank the Robert Bosch Foundation for funding Michaela A. Dippold and Moritz Köster. The study was further supported by the Government Program of Competitive Growth of Kazan Federal University and with the support of the ‘RUDN University program 5-100’.
2.2.7 References
Aguilera-Betti, I., Muñoz, A.A., Stahle, D., Figueroa, G., Duarte, F., González-Reyes, Á., Christie, D., Lara, A., González, M.E., Sheppard, P.R., Sauchyn, D., Moreira-Muñoz, A., Toledo-Guerrero, I., Olea, M., Apaz, P., Fernandez, A., 2017. The First Millennium-Age Araucaria Araucana in Patagonia. Tree-Ring Res. 73, 53–56. https://doi.org/10.3959/1536-1098-73.1.53
Allen, M.F., 2007. Mycorrhizal Fungi: Highways for Water and Nutrients in Arid Soils. Vadose Zone J. 6, 291.
https://doi.org/10.2136/vzj2006.0068
Andrus, N., Tye, A., Nesom, G., Bogler, D., Lewis, C., Noyes, R., Jaramillo, P., Francisco-Ortega, J., 2009. Phylogenetics of Darwiniothamnus (Asteraceae: Astereae) - molecular evidence for multiple origins in the endemic flora of the Galápagos Islands. J. Biogeogr. 36, 1055–1069. https://doi.org/10.1111/j.1365-2699.2008.02064.x
Antunes, P.M., Koch, A.M., Morton, J.B., Rillig, M.C., Klironomos, J.N., 2011. Evidence for functional divergence in arbuscular mycorrhizal fungi from contrasting climatic origins. New Phytol. 189, 507–514. https://doi.org/10.1111/j.1469-8137.2010.03480.x
Armesto, J.J., 2007. The Mediterranean environment of central Chile. Phys. Geogr. S. Am. 7, 184.
Aroca, R., Ruiz-Lozano, J.M., Zamarreño, Á.M., Paz, J.A., García-Mina, J.M., Pozo, M.J., López-Ráez, J.A., 2013. Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J.
Plant Physiol. 170, 47–55. https://doi.org/10.1016/j.jplph.2012.08.020
Balser, T.C., Treseder, K.K., Ekenler, M., 2005. Using lipid analysis and hyphal length to quantify AM and saprotrophic fungal abundance along a soil chronosequence. Soil Biol. Biochem. 37, 601–604. https://doi.org/10.1016/j.soilbio.2004.08.019 Bates, D., Mächler, M., Bolker, B., Walker, S., 2015. Fitting Linear Mixed-Effects Models Using lme4. J. Stat. Softw. 67.
https://doi.org/10.18637/jss.v067.i01
Bennett, A.E., Classen, A.T., 2020. Climate change influences mycorrhizal fungal–plant interactions, but conclusions are limited by geographical study bias. Ecology. https://doi.org/10.1002/ecy.2978
Bernhard, N., Moskwa, L.-M., Schmidt, K., Oeser, R.A., Aburto, F., Bader, M., Baumann, K., von Blanckenburg, F., Boy, J., van den Brink, L., Brucker, E., Büdel, B., Canessa, R., Dippold, M.A., Ehlers, T.A., Fuentes, J.P., Godoy, R., Jung, P., Karsten, U., Köster, M., Kuzyakov, Y., Leinweber, P., Neidhardt, H., Matus, F., Mueller, C.W., Oelmann, Y., Oses, R., Osses, P., Paulino, L., Samolov, E., Schaller, M., Schmid, M., Spielvogel, S., Spohn, M., Stock, S., Stroncik, N., Tielbörger, K., Übernickel, K., Scholten, T., Seguel, O., Wagner, D., Kühn, P., 2018. Pedogenic and microbial interrelations to regional climate and local topography: new insights from a climate gradient (arid to humid) along the Coastal Cordillera of Chile. Catena.
Bligh, E.G., Dyer, W.J., 1959. A Rapid Method of Total Lipid Extraction and Purification. Can. J. Biochem. Physiol. 37, 911–917.
https://doi.org/10.1139/y59-099
Bowles, T.M., Jackson, L.E., Cavagnaro, T.R., 2018. Mycorrhizal fungi enhance plant nutrient acquisition and modulate nitrogen loss with variable water regimes. Glob. Change Biol. 24, e171–e182. https://doi.org/10.1111/gcb.13884
Bristiel, P., Roumet, C., Violle, C., Volaire, F., 2019. Coping with drought: root trait variability within the perennial grass Dactylis glomerata captures a trade-off between dehydration avoidance and dehydration tolerance. Plant Soil 434, 327–342.
https://doi.org/10.1007/s11104-018-3854-8
Brundrett, M.C., Tedersoo, L., 2018. Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol.
220, 1108–1115. https://doi.org/10.1111/nph.14976
Bücking, H., Kafle, A., 2015. Role of Arbuscular Mycorrhizal Fungi in the Nitrogen Uptake of Plants: Current Knowledge and Research Gaps. Agronomy 5, 587–612. https://doi.org/10.3390/agronomy5040587
Cavagnaro, T.R., Bender, S.F., Asghari, H.R., Heijden, M.G.A. van der, 2015. The role of arbuscular mycorrhizas in reducing soil nutrient loss. Trends Plant Sci. 20, 283–290. https://doi.org/10.1016/j.tplants.2015.03.004
Cole, C.V., Olsen, S.R., Scott, C.O., 1953. The Nature of Phosphate Sorption by Calcium Carbonate. Soil Sci. Soc. Am. J. 17, 352–
356. https://doi.org/10.2136/sssaj1953.03615995001700040013x
Comas, L.H., Becker, S.R., Cruz, V.M.V., Byrne, P.F., Dierig, D.A., 2013. Root traits contributing to plant productivity under drought. Front. Plant Sci. 4. https://doi.org/10.3389/fpls.2013.00442
Delavaux, C.S., Smith-Ramesh, L.M., Kuebbing, S.E., 2017. Beyond nutrients: a meta-analysis of the diverse effects of arbuscular mycorrhizal fungi on plants and soils. Ecology 98, 2111–2119. https://doi.org/10.1002/ecy.1892
de Vries, F.T., Brown, C., Stevens, C.J., 2016. Grassland species root response to drought: consequences for soil carbon and nitrogen availability. Plant Soil 409, 297–312. https://doi.org/10.1007/s11104-016-2964-4
di Castri, F., Hajek, E.R., 1976. Bioclimatologia de Chile. Vicerrectoria Acad. Univ. Catol. Chile 163.
Diehl, P., Fontenla, S., 2010. Arbuscular mycorrhizal infection in two morphological root types of Araucaria araucana (Molina) K.
Koch. Rev. Argent. Microbiol. 42, 133–137.
Dippold, M.A., Kuzyakov, Y., 2016. Direct incorporation of fatty acids into microbial phospholipids in soils: Position-specific labeling tells the story. Geochim. Cosmochim. Acta 174, 211–221. https://doi.org/10.1016/j.gca.2015.10.032
Fellbaum, C.R., Gachomo, E.W., Beesetty, Y., Choudhari, S., Strahan, G.D., Pfeffer, P.E., Kiers, E.T., Bucking, H., 2012. Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. 109, 2666–2671. https://doi.org/10.1073/pnas.1118650109
Fick, S.E., Hijmans, R.J., 2017. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas: New Climate Surfaces for Global Land Areas. Int. J. Climatol. 37, 4302–4315. https://doi.org/10.1002/joc.5086
Fitter, A.H., 1991. Costs and benefits of mycorrhizas: Implications for functioning under natural conditions. Experientia 47, 350–
355. https://doi.org/10.1007/BF01972076
Frostegård, A., Bååth, E., 1996. The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol.
Fertil. Soils 22, 59–65. https://doi.org/10.1007/BF00384433
Frostegård, å., Tunlid, A., Bååth, E., 1991. Microbial biomass measured as total lipid phosphate in soils of different organic content.
J. Microbiol. Methods 14, 151–163. https://doi.org/10.1016/0167-7012(91)90018-L
Godoy, R., Romero, R., Carrillo, R., 1994. Estatus micotrófico de la flora vascular en bosques de coníferas nativas del sur de Chile.
Rev Chil Hist Nat 67, 209–220.
Gunina, A., Dippold, M.A., Glaser, B., Kuzyakov, Y., 2014. Fate of low molecular weight organic substances in an arable soil:
From microbial uptake to utilisation and stabilisation. Soil Biol. Biochem. 77, 304–313.
https://doi.org/10.1016/j.soilbio.2014.06.029
He, M., Dijkstra, F.A., 2014. Drought effect on plant nitrogen and phosphorus: a meta-analysis. New Phytol. 204, 924–931.
https://doi.org/10.1111/nph.12952
Hodge, A., 2009. Root decisions. Plant Cell Environ. 32, 628–640. https://doi.org/10.1111/j.1365-3040.2008.01891.x
Hodge, A., 2004. The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol. 162, 9–24.
https://doi.org/10.1111/j.1469-8137.2004.01015.x
Hodge, A., Fitter, A.H., 2010. Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proc. Natl. Acad. Sci. 107, 13754–13759. https://doi.org/10.1073/pnas.1005874107 Hothorn, T., Bretz, F., Westfall, P., 2008. Simultaneous Inference in General Parametric Models. Biom J 50, 346–363.
Johnson, N.C., Rowland, D.L., Corkidi, L., Egerton-Warburton, L.M., Allen, E.B., 2003. Nitrogen Enrichment Alters Mycorrhizal Allocation at Five Mesic to Semiarid Grasslands. Ecology 84, 1895–1908. https://doi.org/10.1890/0012-9658(2003)084[1895:NEAMAA]2.0.CO;2
Kassambara, A., Mundt, F., 2017. factoextra: Extract and Visualize the Results of Multivariate Data Analyses.
Khalvati, M.A., Hu, Y., Mozafar, A., Schmidhalter, U., 2005. Quantification of Water Uptake by Arbuscular Mycorrhizal Hyphae and its Significance for Leaf Growth, Water Relations, and Gas Exchange of Barley Subjected to Drought Stress. Plant Biol. 7, 706–712. https://doi.org/10.1055/s-2005-872893
Köhl, L., van der Heijden, M.G.A., 2016. Arbuscular mycorrhizal fungal species differ in their effect on nutrient leaching. Soil Biol. Biochem. 94, 191–199. https://doi.org/10.1016/j.soilbio.2015.11.019
König, N., Versuchsanstalt, N.F., Analytik, M. des G.F., Stellvertreter, G., Blum, U., für Wald, B.L., Sachsen, L., Mitglieder, D., Bussian, B., Groeticke, K., 2005. Eine Loseblatt-Sammlung der Analysemethoden im Forstbereich Herausgegeben vom Gutachterausschuss Forstliche Analytik.
Kuzyakov, Y., Domanski, G., 2000. Carbon input by plants into the soil. Review. J. Plant Nutr. Soil Sci. 163, 421–431.
Lê, S., Josse, J., Husson, F., 2008. FactoMineR : An R Package for Multivariate Analysis. J. Stat. Softw. 25.
https://doi.org/10.18637/jss.v025.i01
Leigh, J., Hodge, A., Fitter, A.H., 2009. Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytol. 181, 199–207. https://doi.org/10.1111/j.1469-8137.2008.02630.x
Leuschner, C., Hertel, D., Schmid, I., Koch, O., Muhs, A., Hölscher, D., 2004. Stand fine root biomass and fine root morphology in old-growth beech forests as a function of precipitation and soil fertility. Plant Soil 258, 43–56.
https://doi.org/10.1023/B:PLSO.0000016508.20173.80
Li, H., Smith, S.E., Holloway, R.E., Zhu, Y., Smith, F.A., 2006. Arbuscular mycorrhizal fungi contribute to phosphorus uptake by wheat grown in a phosphorus-fixing soil even in the absence of positive growth responses. New Phytol. 172, 536–543.
https://doi.org/10.1111/j.1469-8137.2006.01846.x
Marschner, P., Rengel, Z., 2012. Nutrient Availability in Soils, in: Marschner’s Mineral Nutrition of Higher Plants. Elsevier, pp.
315–330. https://doi.org/10.1016/B978-0-12-384905-2.00012-1
Marulanda, A., Azcon, R., Ruiz-Lozano, J.M., 2003. Contribution of six arbuscular mycorrhizal fungal isolates to water uptake by Lactuca sativa plants under drought stress. Physiol. Plant. 119, 526–533. https://doi.org/10.1046/j.1399-3054.2003.00196.x
McCormack, M.L., Iversen, C.M., 2019. Physical and Functional Constraints on Viable Belowground Acquisition Strategies. Front.
Plant Sci. 10, 1215. https://doi.org/10.3389/fpls.2019.01215
Muñoz, M.R., Squeo, F.A., León, M.F., Tracol, Y., Gutiérrez, J.R., 2008. Hydraulic lift in three shrub species from the Chilean coastal desert. J. Arid Environ. 72, 624–632. https://doi.org/10.1016/j.jaridenv.2007.09.006
Nadelhoffer, K.J., Raich, J.W., 1992. Fine Root Production Estimates and Belowground Carbon Allocation in Forest Ecosystems.
Ecology 73, 1139–1147. https://doi.org/10.2307/1940664
Ngosong, C., Gabriel, E., Ruess, L., 2012. Use of the Signature Fatty Acid 16:1 ω 5 as a Tool to Determine the Distribution of Arbuscular Mycorrhizal Fungi in Soil. J. Lipids 2012, 1–8. https://doi.org/10.1155/2012/236807
Nicolson, T.H., 1955. The mycotrophic habit in grasses. University of Nottingham.
Nicotra, A., Babicka, N., Westoby, M., 2002. Seedling root anatomy and morphology: an examination of ecological differentiation with rainfall using phylogenetically independent contrasts. Oecologia 130, 136–145.
https://doi.org/10.1007/s004420100788
Nilsson, L.O., Giesler, R., Bååth, E., Wallander, H., 2004. Growth and biomass of mycorrhizal mycelia in coniferous forests along short natural nutrient gradients. New Phytol. 165, 613–622. https://doi.org/10.1111/j.1469-8137.2004.01223.x
Oeser, R.A., Stroncik, N., Moskwa, L.-M., Bernhard, N., Schaller, M., Canessa, R., van den Brink, L., Köster, M., Brucker, E., Stock, S., Fuentes, J.P., Godoy, R., Matus, F., Oses Pedraza, R., Osses McIntyre, P., Paulino, L., Seguel, O., Bader, M.Y., Boy, J., Dippold, M.A., Ehlers, T.A., Kühn, P., Kuzyakov, Y., Leinweber, P., Scholten, T., Spielvogel, S., Spohn, M., Übernickel, K., Tielbörger, K., Wagner, D., von Blanckenburg, F., 2018. Chemistry and Microbiology of the Critical Zone along a steep climate and vegetation gradient in the Chilean Coastal Cordillera. Catena.
Olsson, P.A., 1999. Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. FEMS Microbiol. Ecol. 29, 303–310. https://doi.org/10.1111/j.1574-6941.1999.tb00621.x
Olsson, P.A., Bååth, E., Jakobsen, I., Söderström, B., 1995. The use of phospholipid and neutral lipid fatty acids to estimate biomass of arbuscular mycorrhizal fungi in soil. Mycol. Res. 99, 623–629. https://doi.org/10.1016/S0953-7562(09)80723-5 Olsson, P.A., Francis, R., Read, D.J., Söderström, B., 1998. Growth of arbuscular mycorrhizal mycelium in calcareous dune sand
and its interaction with other soil microorganisms as estimated by measurement of specific fatty acids 8.
Olsson, P.A., van Aarle, I.M., Gavito, M.E., Bengtson, P., Bengtsson, G., 2005. 13C Incorporation into Signature Fatty Acids as an Assay for Carbon Allocation in Arbuscular Mycorrhiza. Appl. Environ. Microbiol. 71, 2592–2599.
https://doi.org/10.1128/AEM.71.5.2592-2599.2005
Ostonen, I., Püttsepp, ü., Biel, C., Alberton, O., Bakker, M.R., Lõhmus, K., Majdi, H., Metcalfe, D., Olsthoorn, A.F.M., Pronk, A., Vanguelova, E., Weih, M., Brunner, I., 2007. Specific root length as an indicator of environmental change. Plant Biosyst.
- Int. J. Deal. Asp. Plant Biol. 141, 426–442. https://doi.org/10.1080/11263500701626069
Parniske, M., 2008. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol. 6, 763–775.
https://doi.org/10.1038/nrmicro1987
Pérez-Ramos, I.M., Volaire, F., Fattet, M., Blanchard, A., Roumet, C., 2013. Tradeoffs between functional strategies for resource-use and drought-survival in Mediterranean rangeland species. Environ. Exp. Bot. 87, 126–136.
https://doi.org/10.1016/j.envexpbot.2012.09.004
R Core Team, 2019. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
Reich, P.B., 2014. The world-wide ‘fast-slow’ plant economics spectrum: a traits manifesto. J. Ecol. 102, 275–301.
https://doi.org/10.1111/1365-2745.12211
Rillig, M.C., Mummey, D.L., 2006. Mycorrhizas and soil structure. New Phytol. 171, 41–53. https://doi.org/10.1111/j.1469-8137.2006.01750.x
Ryan, M.H., Tibbett, M., Edmonds-Tibbett, T., Suriyagoda, L.D.B., Lambers, H., Cawthray, G.R., Pang, J., 2012. Carbon trading for phosphorus gain: the balance between rhizosphere carboxylates and arbuscular mycorrhizal symbiosis in plant phosphorus acquisition: Carbon trading for phosphorus gain. Plant Cell Environ. 35, 2170–2180.
https://doi.org/10.1111/j.1365-3040.2012.02547.x
Sala, O.E., Golluscio, R.A., Lauenroth, W.K., Roset, P.A., 2012. Contrasting nutrient-capture strategies in shrubs and grasses of a Patagonian arid ecosystem. J. Arid Environ. 82, 130–135. https://doi.org/10.1016/j.jaridenv.2012.02.015
Schaller, M., Ehlers, T.A., Lang, K.A.H., Schmid, M., Fuentes-Espoz, J.P., 2018. Addressing the contribution of climate and vegetation cover on hillslope denudation, Chilean Coastal Cordillera (26°–38°S). Earth Planet. Sci. Lett. 489, 111–122.
https://doi.org/10.1016/j.epsl.2018.02.026
Schwinning, S., Sala, O.E., 2004. Hierarchy of responses to resource pulses in arid and semi-arid ecosystems. Oecologia 141, 211–
220. https://doi.org/10.1007/s00442-004-1520-8
Smith, S.E., Smith, F.A., 2011. Roles of Arbuscular Mycorrhizas in Plant Nutrition and Growth: New Paradigms from Cellular to Ecosystem Scales. Annu. Rev. Plant Biol. 62, 227–250. https://doi.org/10.1146/annurev-arplant-042110-103846 Solbrig, O.T., 1966. The South American species of Gutierrezia. Contrib. Gray Herb. Harv. Univ. 3–42.
Solbrig, O.T., 1962. The South American Species of Erigeron. Contrib. Gray Herb. Harv. Univ. 3–79.
Sommer, J., Dippold, M.A., Zieger, S.L., Handke, A., Scheu, S., Kuzyakov, Y., 2017. The tree species matters: Belowground carbon input and utilization in the myco-rhizosphere. Eur. J. Soil Biol. 81, 100–107.
https://doi.org/10.1016/j.ejsobi.2017.07.001
Trabucco, A., Zomer, R.J., 2018. Global Aridity Index and Potential Evapo-Transpiration (ET0) Climate Database v2. CGIAR Consortium for Spatial Information (CGIAR-CSI). Published online, available from the CGIAR-CSI GeoPortal at https://cgiarcsi.community 10.
Treseder, K.K., 2004. A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies.
New Phytol. 164, 347–355. https://doi.org/10.1111/j.1469-8137.2004.01159.x
Valdebenito, H., Lowrey, T.K., Stuessy, T.F., 1986. A New Species of Erigeron (Compositae: Astereae) from Chile. Brittonia 38, 1. https://doi.org/10.2307/2807408
van der Heijden, M.G.A. van der, 2010. Mycorrhizal fungi reduce nutrient loss from model grassland ecosystems. Ecology 91, 1163–1171. https://doi.org/10.1890/09-0336.1
van Dongen, R., Scherler, D., Wittmann, H., von Blanckenburg, F., 2019. Cosmogenic 10 Be in river sediment: where grain size matters and why. Earth Surf. Dyn. 7, 393–410. https://doi.org/10.5194/esurf-7-393-2019
Veblen, T.T., 1982. Regeneration Patterns in Araucaria araucana Forests in Chile. J. Biogeogr. 9, 11.
https://doi.org/10.2307/2844727
Vierheilig, H., Coughlan, A.P., Wyss, U., Piche, Y., 1998. Ink and Vinegar, a Simple Staining Technique for Arbuscular-Mycorrhizal Fungi 64, 4.
Wright, D.P., Read, D.J., Scholes, J.D., 1998. Mycorrhizal sink strength influences whole plant carbon balance of Trifolium repens L. Plant Cell Environ. 21, 881–891. https://doi.org/10.1046/j.1365-3040.1998.00351.x
.